Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

Abstract

Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and characterised facultatively parthenogenetic populations of the North American stick insect Timema douglasi, a species in which only obligately parthenogenetic populations were known so far. These populations comprised three genetic lineages. Females from all lineages were capable of parthenogenesis (with variable efficiency) but their propensity to reproduce sexually after mating varied extensively. In all three lineages, parthenogenesis resulted in the complete loss of heterozygosity in a single generation. Obligately parthenogenetic Timema have also lost all heterozygosity, suggesting that the transition to obligate parthenogenesis did not require a modification of the proximate mechanism, but rather involved a gradual increase in frequency. We speculate that facultative parthenogenesis may often be transient and be replaced by obligate strategies (either sex or parthenogenesis) because of a trade-off between the efficiency of the two reproductive modes. Such a trade-off could help explain why facultative parthenogenesis is rare among animals, despite its potential to combine the known benefits of sex and parthenogenesis.

Evolution of alternative reproductive systems inBacillusstick insects

“…In some of the egg nuclei, the chromatids replicate but do not segregate, which results in a diploid, but fully homozygous embryo. The low levels of heterozygosity that we observed in these populations are likely an artifact caused by structural variants, as has been observed elsewhere (Jaegle et al, 2023;Jaron et al, 2022;Larose et al, 2023). In B. atticus, heterozygosity was higher than in all sexual species, consistent with the hypothesis that this species might be of hybrid origin, but involving currently unknown species or populations (Bullini & Nascetti, 1989).…”

“…The fact that it derived its mitochondria from B. atticus implies that this species was its maternal ancestor and that B. atticus females have retained the capacity to reproduce sexually. Taken together with the documented production of rare males in this species (Scali, 2013), this opens the possibility for cryptic sex in this otherwise obligate parthenogenetic species, which could contribute to its long-term maintenance (as for example in some species of Timema stick insects; Freitas et al, 2023;Larose et al, 2023).…”

“…The fact that the genus Bacillus encompasses the full breadth of reproductive modes found in animals raises the question of whether they are predisposed to unusual reproduction. Facultative parthenogenesis appears to be widespread in stick insects and often (but not always) occurs via gamete duplication (White, 1973;Larose et al, 2023), suggesting that it might be ancestral to Phasmatodea. there are specific features in their respective genomes that lead to unusual reproduction.…”

Evidence for cryptic sex in parthenogenetic stick insects of the genus Timema

“…This should result in the fixation of one or few clones (genotypes), with minor genetic differences between individuals within clonal lineages. In Timema , strict parthenogenesis would further be associated with very low heterozygosity for all individuals in a population, since their parthenogenesis mechanism leads to the complete or largely complete loss of heterozygosity every generation [ 31 , 32 ]. On the other hand, if parthenogenetic Timema populations are undergoing rare sex we would expect to see an increase in the genotypic diversity, and perhaps some individuals with elevated heterozygosity, which would indicate that they were produced via sex.…”

“…These lineages vary in age, and the oldest parthenogenetic Timema is thought to have been reproducing via parthenogenesis for over 1 Myr [ 30 ], making them an ‘old' asexual species. Parthenogenetic Timema are very homozygous as they most likely reproduce via a form of automictic parthenogenesis where heterozygosity is completely lost each generation [ 31 , 32 ]. Rare males have been found in four of the five described parthenogenetic Timema species [ 28 , 29 , 33 ], and these rare ‘parthenogenetic' males present normal male reproductive organs, and can mate and produce offspring with sexual sister-species females, although with reduced fertility [ 33 ].…”